Retrieved emotional context influences hippocampal involvement during recognition of neutral memories

Highlights

• Effect of arousing context on neutral content memory at different delays was tested.

• Confident content memory was associated more with arousing context at retrieval.

• Attributing arousing context to neutral content at retrieval activated hippocampus.

Abstract

It is well documented that emotionally arousing experiences are better remembered than mundane events. This is thought to occur through hippocampus-amygdala crosstalk during encoding, consolidation, and retrieval. Here we investigated whether emotional events (context) also cause a memory benefit for simultaneously encoded non-arousing contents and whether this effect persists after a delay via recruitment of a similar hippocampus-amygdala network. Participants studied neutral pictures (content) encoded together with either an arousing or a neutral sound (that served as context) in two study sessions three days apart. Memory was tested in a functional magnetic resonance scanner directly after the second study session. Pictures recognised with high confidence were more often thought to have been associated with an arousing than with a neutral context, irrespective of the veridical source memory. If the retrieved context was arousing, an area in the hippocampus adjacent to the amygdala exhibited heightened activation and this area increased functional connectivity with the parahippocampal gyrus, an area known to process pictures of scenes. These findings suggest that memories can be shaped by the retrieval act. Memory structures may be recruited to a higher degree when an arousing context is retrieved, and this may give rise to confident judgments of recognition for neutral pictures even after a delay.

Introduction

Memories for emotional or arousing events are remembered well and are often highly vivid even long after their occurrence (for reviews: Cahill and McGaugh (1998), Christianson (1992), Kensinger and Corkin (2004), LaBar and Cabeza (2006), Phelps (2006)). The hippocampus is a critical brain structure for encoding and retrieval of newly learned information (Alvarez and Squire, 1994, Moscovitch et al., 2005, Nadel and Moscovitch, 1997, Squire, 1992). The amygdala is considered to up-regulate hippocampal processing during encoding, consolidation (McGaugh, 2006, Richardson et al., 2004), and retrieval (Dolcos et al., 2005, Ritchey et al., 2008, Sharot et al., 2007, Smith et al., 2005, Smith et al., 2006, Smith et al., 2004, Sterpenich et al., 2009) leading to enhanced memory for arousing events (LaBar and Phelps, 1998). However, the neural mechanisms via which emotion contributes to enhanced memory retrieval are unclear as they are difficult to isolate. First, emotional retrieval cues can inherently evoke online processing of sensory information that in turn evokes emotional responses and can influence retrieval. Second, mnemonic mechanisms may reinstate an emotional experience that occurred during encoding and influence retrieval. One way to isolate the neural mechanisms underlying the retrieval of emotion from perception evoked responses is to use neutral cues that have been associated with emotional context during encoding to test the emotional memory.

Memories for neutral content can be influenced by an arousing context at encoding. For instance, emotional context, such as emotional background pictures and emotional context sentences, can positively influence the recognition of neutral pictures/words embedded in these emotional contexts when tested in short succession (Maratos and Rugg, 2001, Smith et al., 2004). The previous studies also investigated the neural responses at retrieval shortly after encoding. They observed heightened involvement of the hippocampus and amygdala for retrieval of neutral contents embedded in emotional contexts, which is suggestive of enhanced memory and emotion processing at the time of retrieval for neutral items arising from their study history. For a longer delay, memory persistence for neutral items encoded under a threat of shock has been shown (Dunsmoor et al., 2014, Dunsmoor et al., 2015), but less is known about the neural responses at the time of delayed retrieval.

Retrieved memories are not always veridical. Memories of emotionally arousing events are often vivid, detailed and accompanied by a high feeling of confidence, despite potential inaccuracy (Neisser and Harsch, 1992, Talarico and Rubin, 2003). Thus, if a retrieved memory is thought to have been encoded in an arousing context, this may enhance the subjective confidence for the retrieved memory, even though this may not result from a proper reconstruction of the past event. The hippocampus has been reported to show more activity when the retrieved memory is accompanied by a feeling of recollection compared to a feeling of familiarity (Diana et al., 2007a, Diana et al., 2007b, Weis et al., 2004). Moreover, item-emotion binding via the amygdala has been suggested to be the key for persistence of emotional memories (Yonelinas and Ritchey, 2015). This raises the question whether hippocampal and amygdala involvement at retrieval may be influenced by the retrieved emotional association independent of veridical accuracy.

In the current study, we asked whether an arousing context at encoding influences the retrieval of memory for associated neutral content, and whether this potential influence changes as a function of time. Furthermore, we asked whether the memory of neutral content is modulated by the encoded and retrieved context. To address these questions, participants studied two sets of neutral pictures (content) experienced together with either an unpleasant arousing or a neutral non-arousing sound (context) at two occasions three days apart. To observe neural correlates of retrieval and the possible changes with time, we tested recognition memory for the pictures (content memory) and cued-recall of the associated sounds (context memory) for both recently (same day) and remotely (three days earlier) studied stimulus sets. Neural responses were recorded using functional magnetic resonance imaging (fMRI) during the retrieval session. We predicted enhanced memory for neutral content encoded within an arousing context over a non-arousing context, and possible influences of the encoded and retrieved context on the neural mechanisms associated with retrieval of neutral content.